Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.

Disruption of T cell memory during severe immune suppression results in reactivation of chronic viral infections, such as Epstein Barr virus (EBV) and Cytomegalovirus (CMV). How different subsets of memory T cells contribute to the protective immunity against these viruses remains poorly defined. In...

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Main Authors: Heng Giap Woon, Asolina Braun, Jane Li, Corey Smith, Jarem Edwards, Frederic Sierro, Carl G Feng, Rajiv Khanna, Michael Elliot, Andrew Bell, Andrew D Hislop, Stuart G Tangye, Alan B Rickinson, Thomas Gebhardt, Warwick J Britton, Umaimainthan Palendira
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-08-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005799&type=printable
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author Heng Giap Woon
Asolina Braun
Jane Li
Corey Smith
Jarem Edwards
Frederic Sierro
Carl G Feng
Rajiv Khanna
Michael Elliot
Andrew Bell
Andrew D Hislop
Stuart G Tangye
Alan B Rickinson
Thomas Gebhardt
Warwick J Britton
Umaimainthan Palendira
author_facet Heng Giap Woon
Asolina Braun
Jane Li
Corey Smith
Jarem Edwards
Frederic Sierro
Carl G Feng
Rajiv Khanna
Michael Elliot
Andrew Bell
Andrew D Hislop
Stuart G Tangye
Alan B Rickinson
Thomas Gebhardt
Warwick J Britton
Umaimainthan Palendira
author_sort Heng Giap Woon
collection DOAJ
description Disruption of T cell memory during severe immune suppression results in reactivation of chronic viral infections, such as Epstein Barr virus (EBV) and Cytomegalovirus (CMV). How different subsets of memory T cells contribute to the protective immunity against these viruses remains poorly defined. In this study we examined the compartmentalization of virus-specific, tissue resident memory CD8+ T cells in human lymphoid organs. This revealed two distinct populations of memory CD8+ T cells, that were CD69+CD103+ and CD69+CD103-, and were retained within the spleen and tonsils in the absence of recent T cell stimulation. These two types of memory cells were distinct not only in their phenotype and transcriptional profile, but also in their anatomical localization within tonsils and spleen. The EBV-specific, but not CMV-specific, CD8+ memory T cells preferentially accumulated in the tonsils and acquired a phenotype that ensured their retention at the epithelial sites where EBV replicates. In vitro studies revealed that the cytokine IL-15 can potentiate the retention of circulating effector memory CD8+ T cells by down-regulating the expression of sphingosine-1-phosphate receptor, required for T cell exit from tissues, and its transcriptional activator, Kruppel-like factor 2 (KLF2). Within the tonsils the expression of IL-15 was detected in regions where CD8+ T cells localized, further supporting a role for this cytokine in T cell retention. Together this study provides evidence for the compartmentalization of distinct types of resident memory T cells that could contribute to the long-term protection against persisting viral infections.
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spelling doaj-art-552bcd3b75c8474db486435ca84dbb1b2025-08-20T02:03:19ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742016-08-01128e100579910.1371/journal.ppat.1005799Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.Heng Giap WoonAsolina BraunJane LiCorey SmithJarem EdwardsFrederic SierroCarl G FengRajiv KhannaMichael ElliotAndrew BellAndrew D HislopStuart G TangyeAlan B RickinsonThomas GebhardtWarwick J BrittonUmaimainthan PalendiraDisruption of T cell memory during severe immune suppression results in reactivation of chronic viral infections, such as Epstein Barr virus (EBV) and Cytomegalovirus (CMV). How different subsets of memory T cells contribute to the protective immunity against these viruses remains poorly defined. In this study we examined the compartmentalization of virus-specific, tissue resident memory CD8+ T cells in human lymphoid organs. This revealed two distinct populations of memory CD8+ T cells, that were CD69+CD103+ and CD69+CD103-, and were retained within the spleen and tonsils in the absence of recent T cell stimulation. These two types of memory cells were distinct not only in their phenotype and transcriptional profile, but also in their anatomical localization within tonsils and spleen. The EBV-specific, but not CMV-specific, CD8+ memory T cells preferentially accumulated in the tonsils and acquired a phenotype that ensured their retention at the epithelial sites where EBV replicates. In vitro studies revealed that the cytokine IL-15 can potentiate the retention of circulating effector memory CD8+ T cells by down-regulating the expression of sphingosine-1-phosphate receptor, required for T cell exit from tissues, and its transcriptional activator, Kruppel-like factor 2 (KLF2). Within the tonsils the expression of IL-15 was detected in regions where CD8+ T cells localized, further supporting a role for this cytokine in T cell retention. Together this study provides evidence for the compartmentalization of distinct types of resident memory T cells that could contribute to the long-term protection against persisting viral infections.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005799&type=printable
spellingShingle Heng Giap Woon
Asolina Braun
Jane Li
Corey Smith
Jarem Edwards
Frederic Sierro
Carl G Feng
Rajiv Khanna
Michael Elliot
Andrew Bell
Andrew D Hislop
Stuart G Tangye
Alan B Rickinson
Thomas Gebhardt
Warwick J Britton
Umaimainthan Palendira
Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
PLoS Pathogens
title Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
title_full Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
title_fullStr Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
title_full_unstemmed Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
title_short Compartmentalization of Total and Virus-Specific Tissue-Resident Memory CD8+ T Cells in Human Lymphoid Organs.
title_sort compartmentalization of total and virus specific tissue resident memory cd8 t cells in human lymphoid organs
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005799&type=printable
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